KIN10 promotes stomatal development through stabilization of the SPEECHLESS transcription factor

Chao Han,Min Fan,On Sun Lau,Geert De Jaeger,Yanchen Tian,Yan Qiao,Yue Liu,Wen Shi,Lingyan Wang,Zhiping Deng,Ming-Yi Bai

doi:10.1038/s41467-020-18048-w

Abstract

Stomata are epidermal structures that modulate gas exchanges between plants and the atmosphere. The formation of stomata is regulated by multiple developmental and environmental signals, but how these signals are coordinated to control this process remains unclear. Here, we showed that the conserved energy sensor kinase SnRK1 promotes stomatal development under short-day photoperiod or in liquid culture conditions. Mutation of KIN10, the catalytic α-subunit of SnRK1, results in the decreased stomatal index; while overexpression of KIN10 significantly induces stomatal development. KIN10 displays the cell-type-specific subcellular location pattern. The nuclear-localized KIN10 proteins are highly enriched in the stomatal lineage cells to phosphorylate and stabilize SPEECHLESS, a master regulator of stomatal formation, thereby promoting stomatal development. Our work identifies a module links connecting the energy signaling and stomatal development and reveals that multiple regulatory mechanisms are in place for SnRK1 to modulate stomatal development in response to changing environments.

Highlights

Stomata are epidermal structures that modulate gas exchanges between plants and the atmosphere
The stomatal index of plants grown under the 16 h light/ 8 h dark photoperiod condition was much higher than that of plants grown under the 4 h light/20 h dark photoperiod condition (Fig. 1b)
Treatment with sucrose promoted cell expansion and induced cell division, and led to the increased amounts of stomata in the whole cotyledon and high ratio of clustered stomata (Supplementary Fig. 2a–h). These results indicated that sugar promotes stomatal development under certain conditions, such as low light quantity, short-day photoperiod, or in hypoxic liquid growth media

Summary

Introduction

Stomata are epidermal structures that modulate gas exchanges between plants and the atmosphere. We showed that the conserved energy sensor kinase SnRK1 promotes stomatal development under short-day photoperiod or in liquid culture conditions. The nuclear-localized KIN10 proteins are highly enriched in the stomatal lineage cells to phosphorylate and stabilize SPEECHLESS, a master regulator of stomatal formation, thereby promoting stomatal development. Sucrose non-fermenting[1] (SNF1)-related kinase 1 (SnRK1) is a central energy sensor kinase in plants that is functionally and evolutionarily conserved with SNF1 in yeast and AMP-activated kinase (AMPK) in animals[10,11,12,13]. In stomatal-lineage cells, the nuclearlocalized KIN10 phosphorylated and stabilized SPCH to promote stomatal development. These results demonstrated that fine-tuning of KIN10 activity by environmental and developmental signals optimizes stomatal development in Arabidopsis

Methods

Results

Conclusion